Journal of Molecular Evolution

, Volume 57, Supplement 1, pp S3–S12 | Cite as

Radiation of Extant Marsupials After the K/T Boundary: Evidence from Complete Mitochondrial Genomes

  • Maria A. Nilsson
  • Anette Gullberg
  • Angel E. Spotorno
  • Ulfur Arnason
  • Axel JankeEmail author


The complete mitochondrial (mt) genomes of five marsupial species have been sequenced. The species represent all three South American orders (Didelphimorphia, Paucituberculata, and Microbiotheria). Phylogenetic analysis of this data set indicates that Didelphimorphia is a basal marsupial lineage followed by Paucituberculata. The South American microbiotherid Dromiciops gliroides (monito del monte) groups with Australian marsupials, suggesting a marsupial colonization of Australia on two occasions or, alternatively, a migration of an Australian marsupial lineage to South America. Molecular estimates suggest that the deepest marsupial divergences took place 64–62 million years before present (MYBP), implying that the radiation of recent marsupials took place after the K/T (Cretaceous/Tertiary) boundary. The South American marsupial lineages are all characterized by a putatively nonfunctional tRNA for lysine, a potential RNA editing of the tRNA for asparagine, and a rearrangement of tRNA genes at the origin of light strand replication.


Marsupialia Phylogeny Mitogenomics Dromiciops Caenolestes Rhyncholestes Thylamys Monodelphis 


  1. 1.
    Adachi, J, Hasegawa, M 1996MOLPHY version 2.3: Programs for molecular phylogenetics based on maximum likelihood. Computer Science Monographs 28:1.Inst Stat MathTokyoGoogle Scholar
  2. 2.
    Aplin, KP, Archer, M 1987Recent advances in marsupial systematics with a new syncretic classification.Archer, M eds. Possums and opossums studies in evolution.Surrey Beatty and SonsChipping Norton, New South WalesXVLXXIIGoogle Scholar
  3. 3.
    Arnason, U, Gullberg, A 1996Cytochrome b nucleotide sequences and the identification of five primary lineages of extant cetaceans.Mol Biol Evol13407417PubMedGoogle Scholar
  4. 4.
    Arnason, U, Janke, A 2002Mitogenomic analyses of eutherian relationships.Cytogenet Genome Res962032CrossRefPubMedGoogle Scholar
  5. 5.
    Arnason, U, Gullberg, A, Janke, A, Xu, X 1996Pattern and timing of evolutionary divergences among hominoids based on analyses of complete mtDNAs.J Mol Evol43650661PubMedGoogle Scholar
  6. 6.
    Arnason, U, Gullberg, A, Janke, A 1998Molecular timing of primate divergences as estimated from two non-primate calibration points.J Mol Evol47718727PubMedGoogle Scholar
  7. 7.
    Arnason, U, Gullberg, A, Gretarsdottir, S, Ursing, B, Janke, A 2000The complete mitochondrial genome of the sperm whale and the establishment of a new molecular reference for estimating eutherian divergence dates.J Mol Evol50569578PubMedGoogle Scholar
  8. 8.
    Arnason, U, Adegoke, JA, Bodin, K, Born, EW, Esa, YB, Gullberg, A, Nilsson, M, Short, RV, Xu, X, Janke, A 2002Mammalian mitogenomic relationships and the root of the eutherian tree.Proc Natl Acad Sci USA99815l8156CrossRefGoogle Scholar
  9. 9.
    Biggers, JD, DeLamater, ED 1965Marsupial spermatozoa pairing in the epididymis of American forms.Nature208402404PubMedGoogle Scholar
  10. 10.
    Cabot, EL, Beckenbach, AT 1989Simultaneous editing of multiple nucleic acid and protein sequences with ESEE.Comput Appl Biosci5233234PubMedGoogle Scholar
  11. 11.
    Cifelli, RL 1993Early Cretaceous mammal from North America and the evolution of marsupial dental characters.Proc Natl Acad Sci USA9094139416PubMedGoogle Scholar
  12. 12.
    Colgan, DJ 1999Phylogenetic studies of marsupials based on phosphoglycerate kinase DNA sequences.Mol Phylogenet Evol111326CrossRefPubMedGoogle Scholar
  13. 13.
    Da Silva, MNF, Patton, JL 1998Molecular phylogeography and the evolution and conservation of Amazonian mammals.Mol Ecol7475486CrossRefPubMedGoogle Scholar
  14. 14.
    Dorner, M, Altmann, M, Paabo, S, Morl, M 2001Evidence for import of a lysyl-tRNA into marsupial mitochondria.Mol Biol Cell1226882698PubMedGoogle Scholar
  15. 15.
    Drummond, A, Strimmer, K 2001PAL: An object-oriented programming library for molecular evolution and phylogenetics.Bioinformatics17662663CrossRefPubMedGoogle Scholar
  16. 16.
    Felsenstein, J 1993Phylogenetic inference programs (PHYLIP).University of Washington, Seattle, and University Herbarium, University of CaliforniaBerkeleyGoogle Scholar
  17. 17.
    Gissi, C, Reyes, A, Pesole, G, Saccone, C 2000Lineage-specific evolutionary rate in mammalian mtDNA.Mol Biol Evol1710221031PubMedGoogle Scholar
  18. 18.
    Godthelp, H, Archer, M, Cifelli, R, Hand, SJ, Gilkeson, CF 1992Earliest known Australian Tertiary mammal fauna.Nature356514516CrossRefGoogle Scholar
  19. 19.
    Harlid, A, Arnason, U 1999Analysis of mitochondrial DNA nest ratite birds within the Neognathae: Supporting a neotenous origin of ratite morphological characters.Proc R Soc London B266305309CrossRefGoogle Scholar
  20. 20.
    Huelsenbeck, JP, Ronquist, F 2001MRBAYES: Bayesian inference of phylogenetic trees.Bioinformatics17754755Google Scholar
  21. 21.
    Janke, A, Paabo, S 1993Editing of a tRNA anticodon in marsupial mitochondria changes its codon recognition.Nucleic Acids Res2115231525PubMedGoogle Scholar
  22. 22.
    Janke, A, Feldmaier-Fuchs, G, Thomas, WK, Pääbo, S, von Haeseler, G 1994The marsupial mitochondrial genome and the evolution of placental mammals.Genetics137243256PubMedGoogle Scholar
  23. 23.
    Janke, A, Gemmell, NJ, Feldmaier-Fuchs, G, von Haeseler, A, Paabo, S 1996The mitochondrial genome of a monotreme—the platypus (Ornithorhynchus anatinus).J Mol Evol42153159PubMedGoogle Scholar
  24. 24.
    Janke, A, Xu, X, Arnason, U 1997The complete mitochondrial genome of the wallaroo (Macropus robustus) and the phylogenetic relationship among Monotremata, Marsupialia and Eutheria.Proc Natl Acad Sci USA9412761281CrossRefPubMedGoogle Scholar
  25. 25.
    Janke, A, Magnell, O, Wiezcorek, G, Westerman, M, Arnason, U 2002Phylogenetic analysis of 18S rDNA and mitochondrial genomes of the wombat, Vombatus ursinus, and the spiny anteater, Tachyglossus aculeatus: Increased support for the Marsupionta hypothesis.J Mol Evol547180PubMedGoogle Scholar
  26. 26.
    Jones, DT, Taylor, WR, Thornton, JM 1992The rapid generation of mutation data matrices from protein sequences.Comp Appl Biosci8275282PubMedGoogle Scholar
  27. 27.
    Killian, JK, Byrd, JC, Jirtle, JV, Munday, BL, Stoskopf, MK, MacDonald, RG, Jirtle, RL 2000M6P/IGF2R imprinting evolution in mammals.Mol Cell5707716PubMedGoogle Scholar
  28. 28.
    Kirsch, JAW, Dickerman, AW, Reig, OA, Springer, MS 1991DNA hybridization evidence for the Australasian affinity of the American marsupial Dromiciops australis.Proc Natl Acad Sci USA8810465l0469PubMedGoogle Scholar
  29. 29.
    Kirsch, JAW, Lapointe, F-J, Springer, MS 1997DNA hybridization studies of marsupials and their implications for metatherian classification.Aust J Zool45211280Google Scholar
  30. 30.
    Kumar, S, Hedges, SB 1998A molecular timescale for vertebrate evolution.Nature392917920PubMedGoogle Scholar
  31. 31.
    Li, ZX, Powell, CMcA 2001An outline of the palaeogeographic evolution of the Australasian region since the beginning of the Neoproterozoic.Earth Sci Rev53237277CrossRefGoogle Scholar
  32. 32.
    Marshall, LG 1979Evolution of metatherian and eutherian (mammalian) characters: A review based on cladistic methodology.Zool J Linn Soc (London)66369410Google Scholar
  33. 33.
    Morl, M, Dorner, M, Paabo, S 1995C to U editing and modifications during the maturation of the mitochondrial tRNA-Asp in marsupials.Nucleic Acids Res2333803384PubMedGoogle Scholar
  34. 34.
    Murphy, WJ, Eizirik, E, O’Brien, SJ, Madsen, O, Scally, M, Douady, CJ, Teeling, E, Ryder, OA, Stanhope, MJ, de Jong, WW 2001Resolution of the early placental mammal radiation using Bayesian phylogenetics.Science29423482351CrossRefPubMedGoogle Scholar
  35. 35.
    Nowak, RM 1991Walker’s mammals of the world, 5th ed.Johns Hopkins University PressBaltimore and LondonGoogle Scholar
  36. 36.
    Paabo, S, Thomas, WK, Whitfield, K, Kumazawa, Y, Wilson, AC 1991Rearrangements of mitochondrial transfer RNA genes in marsupials.J Mol Evol33426430PubMedGoogle Scholar
  37. 37.
    Palma, RE, Spotorno, AE 1999Molecular systematics of marsupials based on the rRNA 12S mitochondrial gene: The phylogeny of Didelphimorphia and of the living fossil microbiotheriid Dromiciops gliroides thomas.Mol Phylogenet Evol13525535CrossRefPubMedGoogle Scholar
  38. 38.
    Phillips, MJ, Lin, YH, Harrison, GL, Penny, D 2001Mitochondrial genomes of a bandicoot and a brushtail possum confirm the monophyly of australidelphian marsupials.Proc R Soc Lond B Biol Sci26815331538CrossRefPubMedGoogle Scholar
  39. 39.
    Retief, JD, Winkfein, RJ, Dixon, GH 1993Evolution of monotremes—The sequences of the protamine P1 genes of platypus and echidna.Eur J Biochem218457461PubMedGoogle Scholar
  40. 40.
    Rougier, GW, Wible, JR, Novacek, MJ 1998Implications of Deltatheridium specimens for early marsupial history.Nature396459463CrossRefPubMedGoogle Scholar
  41. 41.
    Sambrook, J, Fitsch, EF, Maniatis, T 1989Molecular cloning, a laboratory manual, 2nd ed.Cold Spring Harbor Laboratory PressCold Spring Harbor, NYGoogle Scholar
  42. 42.
    Sanderson, MJ 2002Estimating absolute rates of molecular evolution and divergence times: A penalized likelihood approach.Mol Biol Evol19101109PubMedGoogle Scholar
  43. 43.
    Sarich, VM, Wilson, AC 1973Generation time and genomic evolution in primates.Science17911441147PubMedGoogle Scholar
  44. 44.
    Shimodaira, H, Hasegawa, M 1999Multiple comparisons of log-likelihoods with applications to phylogenetic inference.Mol Biol Evol1611141116Google Scholar
  45. 45.
    Spotorno, AE, Marin, JC, Yevenes, M, Walker, LI, Fernandez-Donoso, RF, Pincheira, J, Berrios, MS, Palma, RE 1997Chromosome divergences among American marsupials and the Australian affinities of the American Dromiciops.J Mammal Evol4259269CrossRefGoogle Scholar
  46. 46.
    Springer, MS, Kirsch, JAW, Case, JA 1997The chronicle of marsupial evolution.Givnish, TSytsma, K eds. Molecular evolution and adaptive radiation.Cambridge University PressNew York129161Google Scholar
  47. 47.
    Springer, MS, Westerman, M, Kavanagh, JR, Burk, A, Woodburne, MO, Kao, DJ, Krajewski, C 1998The origin of the Australasian marsupial fauna and the phylogenetic affinities of the enigmatic monito del monte and marsupial mole.Proc R Soc Lond B Biol Sci26523812386CrossRefPubMedGoogle Scholar
  48. 48.
    Strimmer, K, von Haeseler, A 1996Quartet puzzling: A quartet maximum likelihood method for reconstructing tree topologies.Mol Biol Evol13964969Google Scholar
  49. 49.
    Swofford, DL 1998PAUP*. Phylogenetic analysis using parsimony (*and other methods), Version 4.Sinauer AssociatesSunderland, MAGoogle Scholar
  50. 50.
    Szalay, FS 1982A new appraisal of marsupial phylogeny and classification.Archer, M eds. Carnivorous marsupialsRoy Zool Soc New South WalesSydney621640Google Scholar
  51. 51.
    Szalay, FS 1994Evolutionary history of the marsupials and an analysis of osteological characters.Cambridge University PressNew YorkGoogle Scholar
  52. 52.
    Szalay, FS, Sargis, EJ 2001Model-based analysis of postcranial osteology of marsupials from the Palaeocene of Itaboraí (Brazil) and the phylogenetics and biogeography of Metatheria.Geodiversitas2139302Google Scholar
  53. 53.
    Tamura, K, Nei, M 1993Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees.Mol Biol Evol10512526PubMedGoogle Scholar
  54. 54.
    Temple-Smith, P 1987Sperm structure and marsupial phylogeny.Archer, M eds. Possums and opossums studies in evolution.Surrey Beatty and SonsChipping Norton, New South WalesCLXXICXCIIIGoogle Scholar
  55. 55.
    Toyosawa, S, O’hUigin, C, Figueroa, F, Tichy, H, Klein, J 1998Identification and characterization of amelogenin genes in monotremes, reptiles and amphibians.Proc Natl Acad Sci USA951305613061CrossRefPubMedGoogle Scholar
  56. 56.
    Wolstenholme, DR 1992Animal mitochondrial DNA: structure and evolution.Int Rev Cytol141173215PubMedGoogle Scholar
  57. 57.
    Woodburne, MO, Case, JA 1996Dispersal, vicariance, and the Late Cretaceous to early tertiary land mammal biogeography from South America to Australia.J Mammal Evol3121161Google Scholar
  58. 58.
    Woodburne, MO, Zinsmeister, WJ 1982Fossil land mammal from Antarctica.Science218284286Google Scholar
  59. 59.
    Woodburne, MO, Zinsmeister, WJ 1984The first land mammal from Antarctica and its biogeographic implications.J Paleontol58913948Google Scholar

Copyright information

© Springer-Verlag New York LLC 2003

Authors and Affiliations

  • Maria A. Nilsson
    • 1
  • Anette Gullberg
    • 1
  • Angel E. Spotorno
    • 2
  • Ulfur Arnason
    • 1
  • Axel Janke
    • 1
    Email author
  1. 1.Department of Cell and Organism Biology, Division of Evolutionary Molecular SystematicsUniversity of Lund, Sölvegatan 29, S-223 62 LundSweden
  2. 2.Laboratorio de Citogenetica EvolutivaPrograma de Genética Humana, ICBM, Facultad de Medicina, Universidad de Chile, Casilla 70061, Santiago 7Chile

Personalised recommendations